The objective of the present study was to analyze diel variation in the abundance and size of the seabob shrimp Xiphopenaeus kroyeri in the Ubatuba region, state of São Paulo, during the year 2000. In each season of the year, collections were made in the day and at night on 9 transects at depths ranging from 2 to 40 m. The estimated shrimp amount was of 28,878 individuals. Although the catch rate was higher during the day (15,853 shrimp), this did not differ significantly from the catch at night (13,025). The catch rate was higher in daytime on most transects, but was higher at night at locations where fine and very fine sand predominated. The majority of juveniles were caught during the day. The mean size (CL) was 14.43 ± 4.02 mm for day and 14.82 ± 4.28 mm for night samples, and the difference was significant (Student's t-test, df = 2, 429, t = 2.27, p = 0.02). The largest individuals were caught during the night. None of the three models that have been proposed in the literature to account for differences in the diurnal catch pattern of penaeid species can be applied to X. kroyeri. Our results provide evidence that sediment type not only influenced the catch rate in the analyzed periods, but also determined which models might fit the behavior of this species.

The tropical marine shrimp fishery, mainly for penaeid shrimps, is a very old activity. In recent decades, the mechanization of fishing boats and the growth of shrimp fleets have intensified exploitation, which has caused declines and even collapse of these fisheries. In Brazil, with the significant decline of the shrimp Farfantepenaeus spp. since the 1980s (Paiva 1997), the population of X. kroyeri, commonly called as "sete-barbas", became the most important target and is already impacted because of continuous indiscriinate harvesting, especially in the state of São Paulo (Costa et al. 2007).

Sediment type and depth have been emphasized as major variables affecting the distribution of the penaeid shrimps (Dall et al. 1990). Several studies have demonstrated the substrate influence on some shrimp biological processes, since shrimps live on the substrate or buried in it (Fuss Jr and Ogren 1966). The majority of species remains buried during the day and emerge at dusk, i.e., are most active in the period when they are least vulnerable to potential predators (Minello et al. 1987, Laprise and Blader 1992, Sogard and Able 1994, Dall et al. 1990, Negreiros-Fransozo et al. 1999). Moctezuma and Blake (1981) noted that juveniles remain unburied for a longer period than adults do, because they need more food as a result of their high growth rate. In addition, Penn (1984) noted that the type of substrat can affect burying behavior: in locations with silt and clay sediments, the turbidity of the water may be higher, and here the catch does not differ among the periods. In sandy locations, turbidity is lower and the shrimps are more abundant at night.

Xiphopenaeus kroyeri (Heller, 1862) is widely distributed in the western Atlantic (Virginia, USA, to Rio Grande do Sul, Brazil) and the eastern Pacific (Mexico to Peru) (Pérez-Farfante and Kensley 1997). However, recently, Gusmão et al. (2006) demonstrated through molecular data that X. kroyeri is distributed only in the Atlantic, while Xiphopenaeus riveti occurs in the Pacific. X. kroyeri is the second most important fishery resource in abundance in the Southeastern Brazil, and is the most heavily exploited benthic shrimp species on the coast of the state of São Paulo (D'Incao et al. 2002, Castro et al. 2005).

Most studies on X. kroyeri have been focused on their abundance and ecological distribution (Fransozo et al. 2002, Costa et al. 2007, Castilho et al. 2008), population structure, and reproductive biology (Nakagakiand Negreiros-Fransozo 1998, Fransozo etal. 2000, Castro et al. 2005). Studies of the variation in catch and size of the seabob shrimp during the day and night periods are practically nonexistent. The only study of this nature was carried out by Negreiros-Fransozo et al. (1999), in the same region as the present study, for the species of Penaeoidea, although it had been carried out in only two seasons of the year (summer and winter) and at mean depths of 3.5 ± 0.5 m. These authors found that the number of individuals of these species did not differ among the analyzed periods, although larger shrimps were more often found at dusk. At this location, silt and clay predominate (Costa et al. 2007). Although this previous study had been carried through in depths until 3.5 m, one knows that in Ubatuba, which is in the north coast of the state of São Paulo, X. kroyeri was distributed preferentially down to a depth of 25 m (Costa et al. 2007). In the area of the present study, the sediment texture changes with depth, becoming sandier below 15 m (Costa et al. 2007) and, according to the proposal of Penn (1984), these factors can odify the catch pattern of a penaeid shrimp.

Thus, the objective of the present study was to analyze the diel variation in abundance and size of individuals of X. kroyeri that were caught down to a depth of 40 m in the Ubatuba region, on the northern coast of the state of São Paulo. We also investigated whether a change in sediment type might alter the catch rate between the day and night periods. The present study also provided information on the periods and regions that juveniles are more vulnerable to the fishing, therefore serving as framework for the determination and implantation of management plans that propitiate a sustainable fishing.

MATERIALS AND METHODS

Located along the northern coastline of the state of São Paulo, the Ubatuba region is an important area for crustacean research (Mantelatto and Fransozo 2000). The region is unique when compared to other areas along the Brazilian southern coast. This coastal area is enclosed be within a system of inlets, bays, canals, bayous, and rivers bordered by mangroves that together form estuaries rich in nutrients that are favorable for the establishment and development of the marine fauna. In addition, Ubatuba Bay is fairly pristine and used as a standard for comparison with other marine habitats that are strongly influenced by humans (Mantelatto and Fransozo 1999).

The collections were carried out in all four seasons of the year (summer, autumn, winter and spring) in day and night periods, in the Ubatuba region (Fig. 1), during the year 2000. The samples were taken along 9 bottom transects, at depths of 2, 5, 10, 15, 20, 25, 30, 35 and 40 m. We used a commercial fishing boat equipped with two Mexican-type "double rig" nets. The mesh size of the nets was 20 mm knot-to-knot in the body, and 15 mm in the cod end. Trawls were conducted along each transect for 30 minutes, over a distance of approximately 2 kilometers. Specifics nets for the capture of the shrimp-white were used to prevent the capture of the animals buried in the substratum, i.e., with lighter materials and a high number of floats. The boat speed was also changed from 1.5 to 2 knots.

We obtained the total wet weight (in grams) of the X. kroyeri caught in each trawl. We, then, took a random 250-g subsample, and the number of individuals was counted on each transect of each season. Based on the data from the subsample and from the total biomass, it was possible to estimate the number of individuals for each transect, season, and period.

All the individuals in the subsample were measured for carapace length (CL mm) in millimeters and were sexed. Carapace length, means the distance from the orbital angle to the posterior margin ofthe carapace. The reproductive condition ofthe females was determined by the macroscopic observation of the gonads, adapted from Bauer and Lin (1994) and Costa and Fransozo (2004), with four stages of development: IM = immature, RU = rudimentary (adults with undeveloped gonads), ED = developing, and DE = developed. The reproductive status of males was assessed by examining the shape of the petasma, which is fused in adult individuals (Castro et al. 2005).

The sediment was measured on each transect of each season. Details of the methodology are found in Bertinietal. (2001). The abundance of shrimp was compared among the seasons of the year and the transects, by means of analysis of variance (one-way ANOVA, p<0.05), complemented by Tukey's multiple-comparisons test, at the 5% probability level. For each transect and season, the chi-square test (X2) was used to compare the abundance of juveniles and adults between the sampled periods (day and night). The carapace size of individuals in each season and on each transect was compared between the day and night periods, by means of Student's t-test. Data were log-transformed prior to the analysis, to improve their normality (Zar 1999).

RESULTS

The highest mean values of sediment diameter (phiΦ) were found in the transects of 5 to 15-m depth in all seasons (Table I).

The estimated shrimp amount was of 28,878 individuals: 22,993 (80%) in winter, 3,042 (11%) in summer, 2,562 (8%) in autumn, and only 281 (1%) in spring. The largest number of specimens (24,678) was obtained on the 2 and 10-m transects; a total of 4,200 individuals were found on the 15 to 25-m transects. No shrimp were collected on the 30, 35 or 40-m transects. The number of individuals differed between spring and winter (one-way ANOVA, p = 0.01, MS = 4.16 and F = 3.53). The results for the transect comparisons are given in Table II.

Overall, in spite of the higher catch rate during the day (15,853 shrimp), there was a significant difference from the night samples (13,025) (X2 p = 3.48 E-62).

The number of individuals increased at night in spring (205 ind. at night and 76 ind. in daytime - X2: p = 1.40 E-14) and in summer (1,711 ind. at night and 1,331 ind. in daytime - X2, p = 5.58 E-12). In the other seasons, the contrary was observed: in autumn, 977 shrimps were collected at night, and 1,585 during the day (X2, p = 3.07 E-33); and in winter, 10,132 shrimps were caught at night, and 12,861 in daytime (X2, p = 2.04 E-72) (Fig.2).

The number of individuals differed significantly on most transects (X2 (1-m)p = 7.22 E-30; (5-m)p = 8.02 E-30; (10-m) p = 8.11 E-25; (20-m) p = 1.22 E-24; (25-m) p = 3.48 E-10). On nearly all the transects, the abundance was greater during the day. However, this occurred only at the locations with muddier sediments (phi >4). In contrast, at the 20-m depth, shrimps were caught only at night. At this point, the values of (phi) decreased to close to 3, that is, very fine sand predominated (Fig. 3). The same pattern was observed for juveniles, although the catches at the 10 (X2, p = 0.001), 15 (X2, p = 0.02) and 20-m (X2, p = 0.07 E-10) depths differed significantly (Fig. 4).

The overall mean size (CL) of individuals was 14.43 mm in day samples and 14.82 mm in night samples, which is a significant difference (Student's t-test, df = 2429, t = 2.27, p = 0.02). The largest individuals, including all those with a carapace length above 28 mm, were caught at night (Fig. 5).

Comparing the seasons of the year, the mean size of the individuals was larger in night samples, but a statistical difference was apparent only in autumn (Student's t-test, df = 541, t = 2.08, p = 0.03) (Fig. 6). In terms of spatial relationships, except for the 15-m depth, the mean carapace size of adults collected at night was larger than the carapace size found in the day samples. The largest individuals were collected at the deeper localities, 15 and 20 m (Fig. 7).

DISCUSSION

The catch rate of individuals of X. kroyeri was slightly higher in daytime. This result contrasts with the majority of studies on marine shrimps, mainly of the super-family Penaeoidea (see, Fuss Jr and Ogren 1966, Pérez-Farfante 1971, Cobb et al. 1973, Bauer 1985, Scelzo 2003). In the same region of this study, Lopes et al. (unpublished data) found that for two species of pink shrimp, Farfantepenaeus brasiliensis and F. paulensis, larger numbers of them were caught at night.

Diurnal burying activity is common in the majority of penaeids (Bishop et al. 2008). The burrowing behavior of penaeids is a strategy for energy conservation, as well as a means of defense against potential predators (Kutty and Murugopoopathy 1968, Dall et al. 1990). Shrimps that bury themselves in the substrate during the day are protected against predators that feed in this period, and are less active than those that do not bury.

Penn (1984) developed three models for burying behavior, based on studies with penaeids caught in the Gulf of Mexico: Type 1 - Strongly nocturnal, but often inactive or buried at night, although always buried during the day. The species included here are generally fished for in sandy substrates with relatively clear water; Type 2 - Generally nocturnal and continually active at night, and buried during the day but with a tendency to emerge occasionally. These species differ from Type 1 in being generally associated with muddier substrates. Such areas generally have more turbid water; Type 3 -Rarely bury themselves and almost continually active. These are almost exclusively found in areas of river discharge, which are characterized by high turbidity.

For Xiphopenaeus kroyeri, it is difficult to propose a single pattern in conformity with these three models. Our results showed that, the sediment type of the study area, the size of individuals also affected the catch pattern. At 20 m depth, the shrimps were only found at night, the individuals presented largest sizes, and the sediment was composed of sand and, consequently, at this depth, the shrimps would be considered of the Type 1. In contrast, for the shallower depths, the Type 3 pattern could be proposed because there was no great numerical change in catch rate between day and night. Silt and clay predominated at those locations, suggesting that the water there may be more turbid. In this respect, both the juveniles and adults of X. kroyeri showed the same behavior.

Laboratory experiments with X. kroyeri corroborate our proposal, since the shrimps buried themselves during the day and emerged at night in sediments composed of fine and very fine sand. When the shrimps were placed on muddy substrates, they began to burrow, but stopped immediately when the water became turbid. They did not cover themselves completely with sediment, and remained with only their body inside the small hole that they had dug (F.A.M. Freire et al., unpublished data). According to Penn (1984), other penaeid species such as Penaeus indicus H. Milne Edwards, 1837, P. merguiensis De Maan, 1888, and P. setiferus (Linnaeus, 1767) do not burrow in very soft sediments because they are not capable of reversing the water flux that passes through their branchial chamber in order to avoid clogging (Penn 1984).

Seasonally, the wind action in the study region can also modify the pattern of capture of the individuals.

The suspension of the substratum is caused many times because the wind action (Pedersen et al. 1995) and, consequently, increasing the turbidity of the water. In accordance with Castro-Filho et al. (1987), the strongest winds in the winter induces the penetration of Tropical Water straight to the direction to the coast, destroying the seasonal thermocline formed by the action of the South Atlantic Central Water and directing these masses to the continental slope. Although we did not analyze the wind action in the present study, this fact could have favored the increase of the water turbidity in the autumn and winter months and, consequently, allowing the increase of the individuals captured during the day.

With respect to size, our results agree with the findings of Negreiros-Fransozo et al. (1999), who collected the largest individuals at dusk. According to Dall et al. (1990), juvenile penaeid shrimps do not show a strong response of burying behavior in relation to light as the adults do, which are more caught during the night. In part, this hypothesis can be supported here, in that the smaller individuals of X. kroyeri were caught in about the same numbers in both periods, and the larger individuals were collected more often during the night. However, the adults, even smaller-sized ones, when in shallower areas, showed the same behavior as the juveniles. Experimental studies involving these demographic classes in different types of sediment between the day and night periods might elucidate this question.

The abundance of juveniles and adults varies seasonally in the study region (Costa et al. 2007), mainly due to the changes of the monthly temperatures values. The present study corroborates the results above. Moreover, beyond autumn and winter present values of bottom temperatures higher than spring and summer ones (Costa et al. 2007), we also suggest that the highest number of individuals in this period could be the result of the offseason period (March to May) for all the shrimps. In this way, the unification of the closure period as presently proposed for the pink and seabob shrimps is supported by this study.

In general, we can conclude that, for X. kroyeri, the sediment type is the main factor that affects the catch rate during the day and night periods. Nevertheless, other studies involving the comparison of diel catch rates of this shrimp for different demographic classes (juveniles, adult males, and ripe and spent females) in relation to lunar phases and the tidal cycle may contribute to a greater understanding of its behavior.

ACKNOWLEDGMENTS

We are grateful to the "Fundação de Amparo à Pesquisa do Estado de São Paulo" (FAPESP) for providing financial support (#94/4878-8, #97/12108-6, #97/121063, #97/12107/0, and #04/07309-8). We are also thankful to the NEBECC co-workers for their help during field work and to Dr. Janet Reid for her great help with the English language. All experiments conducted in this study comply with current applicable state and federal laws.